Open Access
Translator Disclaimer
1 January 2014 Induced Senescence Promotes the Feeding Activities and Nymph Development of Myzus persicae (Hemiptera: Aphididae) on Potato Plants
Cristina R. Machado-Assefh, Alejandro F. Lucatti, Adriana E. Alvarez
Author Affiliations +
Abstract

The effect of dark-induced senescence on Solanum tuberosum L. (Solanales: Solanaceae) plants was assessed on the feeding behavior and performance of the green peach aphid, Myzus persicae Sulzer (Hemiptera: Aphididae). Senescence was induced by covering the basal part of the plant with a black cloth for 5 d, avoiding the light passage, but keeping the apical buds uncovered. The basal part of control plants was covered with a white nonwoven cloth. The degree of senescence was determined by measuring the chlorophyll content of the covered leaves. The performance and feeding behavior of M. persicae were studied on the uncovered nonsenescent apical leaves. The aphid's performance was evaluated by measuring nymphal mortality and prereproductive time. Aphid feeding behavior was monitored by the electrical penetration graph technique. In plants with dark-induced senescence, the aphids showed a reduction in their prereproductive time. Aphids also spent more time ingesting sap from the phloem than in control plants and performed more test probes after the first sustained ingestion of phloem sap. These data suggest that M. persicae's phloem activities and nymph development benefit from the nutritional enrichment of phloem sap, derived from dark-induced senescence on potato plants. The induced senescence improved plant acceptance by M. persicae through an increase in sap ingestion that likely resulted in a reduction in developmental time.

The green peach aphid, Myzus persicae Sulzer (Hemiptera: Aphididae), is a piercing-sucking insect that ingests plant phloem fluid through modified mouthparts (stylets). To select the host plant, aphids penetrate plant tissue by inserting their stylets between the cell walls of the epidermis and the mesophyll (Tjallingii and Hogen Esch 1993). On the way to the phloem, the cells of the mesophyll may be punctured by the stylets. When aphids reach the sieve tube, they test the cellular content and, if it is preferred, they begin to ingest phloem sap. The process of host acceptance takes several hours, during which the aphid and the plant interact closely (Pollard 1973, Tjallingii and Hogen Esch 1993, Miles 1999, Cherqui and Tjallingii 2000, Tjallingii 2006, Will and van Bel 2006). By using the electrical penetration graph (EPG) method, it has been possible to thoroughly study plant penetration by the aphid's stylets (McLean and Kinsey 1964; Tjallingii 1978, 1985, 1988). EPG signals have been correlated with aphid's activities as well as with tissue locations of the stylet's tips (Tjallingii and Hogen Esch 1993), and thus constitute a valuable tool to study plant and aphid inter and intracellular interactions at the plant tissue level. For example, EPGs have been used to study induction of resistance or susceptibility of the plant by aphids (Prado and Tjallingii 2007), differences in behaviors among the different species and morphs of aphids (Boquel et al. 2011), mechanisms of virus transmission by aphids (Martin et al. 1997, Fereres and Moreno 2009, Tjallingii et al. 2010), and effects of different host plants on behavior of different aphid species (Alvarez et al. 2006, Le Roux et al. 2010).

M. persicae has a broad host range and attacks many economically important plants. It is the primary aphid species infesting potato crops (Kuroli and Lantos 2006), but some examples of plant resistance have been reported. Alvarez et al. (2006, 2014) found that potato cultivar ‘Kardal’ (Solanum tuberosum L., Solanales: Solanaceae) presents resistance against M. persicae, but the resistance diminishes with the age of the leaf and susceptibility is related to the induction of foliar senescence. Kardal has resistance to M. persicae at the phloem level, and M. persicae is not able to colonize the young leaves but can survive and reproduce on mature to senescent leaves.

Foliar senescence is a developmentally programmed degeneration process that constitutes the final step of leaf development (Buchanan Wollaston 1997, Lim et al. 2007). It is an active process and involves a highly regulated decrease in photosynthesis, chloroplast degradation, macromolecule (proteins, nucleic acid sand lipids) degradation, loss of chlorophyll, and nutrient mobilization to different destinations of the plant (Buchanan-Wollaston 1997, Page et al. 2001, Liu et al. 2008). These physiological changes are evident in differential expression of genes related to various functional categories and activation of signaling pathways (He et al. 2002; Buchanan-Wollaston et al. 2003, 2005; Gepstein et al. 2003; Breeze et al. 2008). As a result of protein degradation (i.e., Rubisco), amino acids are mobilized and enrich the phloem sap. In this sense, leaf senescence could favor aphids, as a higher content of amino acids in the sap could stimulate ingestion and improve nutrition.

There is evidence that aphid infestation alters expression of plant genes that are potentially involved in the conversion of the feeding site into metabolic sinks (Moran and Thompson 2001, Moran et al. 2002, Alvarez et al. 2013). This suggests that sap intake by aphids may be hydraulically equivalent to plant sinks, such as fruits or roots. However, the interaction established between the plant and the aphid is more complex than a natural source-sink interaction of plant tissues (Douglas 2003).

In wheat and oat plants infested with Schizaphis graminum (Rondani), the concentration of amino acids, particularly glutamine, increases locally and systemically. The amino acid glutamine is the main form of transport of nitrogen from senescing leaves to sink organs (Kamachi et al. 1992, Watanabe et al. 1997, Buchanan-Wollaston et al. 2003).

It has been demonstrated that a large number of cellular metabolism genes change their expression both in senescence and under aphid herbivory. Many of these differently expressed genes influence changes in the physiological state of the plants, from source to sink, which suggests that aphids manipulate the host plant response for their own benefit. It has also been suggested that these changes are necessary to prepare the feeding site and may mediate the aphid's ability to establish a colony on a particular host plant genotype, thus promoting a plant susceptibility to aphid feeding (Moran and Thompson 2001; Moran et al. 2002; De Vos et al. 2005, 2007; De Vos and Jander 2009; Alvarez et al. 2013). On the other hand, it has also been proposed that plants may use senescence as a resistance mechanism. In Arabidopsis, the hypersenescent phenotype related to constitutive expresser of PR genes5 (cpr 5) hypersenescence1 mutant seems to be associated with the increase on plant resistance on this mutant, as aphids reproduction and growth rate were reduced (Pegadaraju et al. 2005, 2007).

Here, senescence was induced in the basal part of plants to evaluate the effect that it has on aphid’s performance and feeding behavior on the apical uncovered leaves. The hypothesis is that the turnover and remobilization of nutrients from the senescent basal part of the plant improve performance and feeding behavior of M. persicae on S. tuberosum plants, promoting plant acceptance.

Materials and Methods

Plants and Aphids. Potato plant ‘PO 97.11.9’ was used for the experiments because of its susceptibility to M. persicae. This cultivar was provided by the germplasm bank of INTA Balcarce, Buenos Aires, Argentina. The propagation of plants was performed in vitro on Murashige and Skoog medium (pH 5.8) including vitamins and 3% sucrose. After 2 wk, the rooted plantlets were transferred to soil in a growth chamber at 22 ± 3°C, about 70% relative humidity (RH), and a photoperiod of 16:8 (L:D) h. All plants were evaluated in the preflowering stage, and no tuberization processes were evident or ever noticed for the Solanum genotype used.

M. persicae colonies were reared on radish (Raphanus sativus L.). All aphids used in the experiments came from a colony maintained at the Natural Sciences Department, National University of Salta, Argentina. This colony was initiated from a single virginoparous apterous aphid collected in the field in 2009. Colonies were reared in a climate chamber at 22 ± 2°C, 30–40% RH, and a photoperiod of 16:8 (L:D) h to induce parthenogenesis. A new colony was started every week, and newly molted adult apterae aphids were used for the experiments.

Senescence Induction and Chlorophyll Determination. Senescence was induced by covering the basal part of 4-wk-old S. tuberosum plants for 5 d with black cloth bags that block the passage of light but allow gas exchange. The control plants were covered with bags of nonwoven porous white cloth that allow the passage of light and gas exchange. Both in the test plants and control plants, the apical buds remained uncovered until the end of the evaluation. The grade of senescence was determined in the covered leaves by measuring chlorophyll a, chlorophyll b, and total chlorophyll content by spectrophotometry. Chlorophylls were extracted from potato leaves with buffered aqueous acetone (80% v/v containing 2.5 mM buffer phosphate, pH 7.8). Leaf discs were cut (16 mm), weighed, and then ground to complete dissolution in a mortar with 2 ml of buffered acetone. The homogenate was collected and washed three times (each washing with 1.5 ml of the same buffered acetone). After centrifugation, the supernatant was taken to a final volume of 8 ml and absorbance was measured at 663 and 646 nm with a spectrophotometer (MetroLab 325 BD). Chlorophyll content was then calculated and expressed as microgram of chlorophyll per milliliter of solution per gram of fresh foliar tissue as described by Lichtenthaler (1987) and Porra et al. (1989). Chlorophyll content from one randomly chosen leaf of the covered portion of the plant was determined from four randomly selected plants from both the dark-induced and control treatment.

Aphid Performance. The performance of M. persicae on senescent and control plants was evaluated by recording nymphal mortality and prereproductive time (from newly bom nymph to adult). Two recently molted apterous adults (1–3 d old) were transferred together to the uncovered apical leaves and enclosed in 20-mm-diameter clip cages on the abaxial side of the leaves of each plant. Four or five clip cages per plant and eight plants per treatment were used. The cages were placed on the first to fifth fully expanded leaf, counting from the top of the plant, taking care not to break the stem. After 24 h, adults and nymphs were removed, leaving one newly bom nymph per leaf. The condition of this individual, dead or alive, was recorded daily until the production of the first progeny. Experiments were conducted at 22 ± 2°C, approximately 60% RH, and a photoperiod of 16:8 (L:D) h. In total, 35 insects for the senescent plants and 30 for the control plants were evaluated on eight plants for each treatment. Each plant supported four to five cages in the apical uncovered portion of the plant.

Aphid Feeding Behavior: EPG. The DC-EPG technique (Tjallingii 1985, 1988) was used to monitor probing of apterous young adult aphids. Two plants of each treatment were placed in a Faraday cage; probing behavior including ingestion of two aphids on each plant was recorded simultaneously for 6h. Aphids were placed on the abaxial side of a leaf, which was nearly fully expanded in the uncovered bud of senescent and control plants. Before exposure to the plant, the aphid was attached to the electrode. The electrode was a 2- to 3-cm-long gold wire (20 µm in diameter), conductively glued (water-based silver glue) to the dorsum—while immobilized by a vacuum-suction device. The other end of the gold wire was attached to a 3-cm-long copper wire (0.2 mm in diameter) and connected to the input of the head stage amplifier with a 1-GΩ input resistance and 50× gain. The plant electrode, a 2-mm-thick, 10-cm-long copper rod, was inserted into the soil of the potted plant and connected to the plant voltage output of the EPG device (Giga-8, manufactured by Wageningen University, Wageningen, The Netherlands). In addition to the plants, the aphids and the first-stage amplifiers were set up in a Faraday cage. The recording was started immediately after aphid wiring, at 20 ± 2°C, under constant light in the laboratory, and about 1 h after collecting the aphids from the colony. Signals of eight aphids, two per plant on each setup, were acquired and recorded. Data acquisition and waveform analysis were mediated by PROBE 3.0 software (Laboratory of Entomology, Wageningen University, The Netherlands).

EPG Waveforms, Waveform Patterns, and Parameters. The EPG signals were analyzed by distinguishing the following waveform phases, types, or subtypes: 1 ) waveform C, stylet pathway phase; waveform E, phloem phase, was separated into 2) waveform E1, sieve element salivation and 3) waveform E2, phloem sap ingestion with concunent salivation; 4) waveform E1e, putative extracellular watery salivation; 5) waveform F, derailed stylet mechanics (stylet penetration difficulties); and 6) waveform G, active uptake of water from xylem elements (Tjallingii 1990a,b). Waveform events were defined as single, uninterrupted occurrences of any of the above waveform types or subtypes. Waveforms were characterized into five broad categories of EPG variables following the nomenclature of Tjallingii ( http://www.epgsystems.eu): 1) number of times waveforms occurred per insect, 2) average duration of waveform per event or per insect, 3) maximum duration of waveform for each insect, 4) time to the first occurrence of a waveform from the start of the experiment, and 5) number or percentage of aphids performing sustained phloem ingestion (sE2: uninterrupted period of E2 longer than 10 min). These variables were calculated for each plant treatment (BAZ Excel workbook for calculation of Aphid EPG variables by Edgar Schliephake,  http://www.epgsystems.eu/downloads.php). The terminology used for some variables was modified according to Backus et al. (2007) and Sarria et al. (2009).

Statistical Analysis. The content of chlorophyll a, chlorophyll b, and total chlorophyll of basal covered leaves was compared between senescent and control plants using Student's t-test for independent samples. Contrasts were made between the means of covered versus control plants.

Nymphal mortality between senescent and control plants was compared by Fisher’s exact test, and prereproductive time was compared by Mann—Whitney U rank sum test.

The EPG variables were compiled individually for each aphid and then averaged across all insects in each treatment to provide means and SEM. In the case of multiple waveform events or probes, duration was averaged from the average per individual. The Mann—Whitney U rank sum test was used to test for differences between senescent and control data from S. tuberosum because EPG variables did not follow a normal distribution. The Fisher's exact test was applied for the analysis of the number of aphids showing sustained ingestion (E2 event, longer than 10 min) between treatments. All statistical analyses were performed using InfoStat Professional v2011p software ( http://www.infostat.com.ar; Di-Rienzo et al. 2011).

Results

Chlorophyll Determination. Leaves of plants covered with black cloth for 5 d were etiolated and showed a reduced content of chlorophyll a, chlorophyll b, and total chlorophyll when compared with leaves of control plants (Student's t-test, P ≤ 0.05; Fig. 1).

Aphid Performance. Differences were observed on the aphid's performance between plants with dark-induced senescence and control plants. The prereproductive time on the apical uncovered leaves of plants (with induced senescence in the basal leaves) was shorter than on apical uncovered leaves of control plants (Mann—Whitney U-test, P ≤ 0.0027). On the other hand, a small (12%), but nonsignificant, difference (Fisher's exact test, P=0.440) was found for the percentage of nymphs surviving on the plants covered with a black cloth (Table 1).

Feeding Behavior. The EPG variables were classified into five groups as described by Tjallingii ( http://www.epgsystems.eu/downloads.php) considering its relation to the aphid's activity or stylet location in the plant tissue (Table 2). Nonprobing and overall probing behavior during pathway periods (stylet route to the phloem, Table 2, variables 1–7) differed between senescent and control plants only in the number of test probes (stylet withdrawals within 3 min) after first sustained phloem feeding (variable number 4), which was significantly higher for plants with dark-induced senescence.

Fig. 1.

Content of chlorophyll a, chlorophyll b, and total chlorophyll in control versus senescent leaves of S. tuberosum. Different letters indicate statistical differences (Student's t-test, P≤0.05).

f01_01.jpg

Significant differences between the two treatments were found in phloem contact-phase variables. In plants with dark-induced senescence, the number of salivation followed by ingestion (E12) events per insect (Table 2, variable 10) was significantly higher than in control plants. Total time in phloem phase event per insect was significantly longer in senescent-induced plants (Table 2, variable 21), and this was due to a significantly longer time in the phloem sap ingestion phase (Table 2, variable 20). In contrast, the time in phloem salivation (E1, variable 19) did not differ between treatments. The percentage of aphids showing sustained phloem feeding (a period of E2 longer than 10 min) in plants with dark-induced senescence was higher than in the control plants (82 vs. 60%, respectively, Table 2, variable 25). However, this difference was not statistically significant.

Discussion

Senescence is a very complex process involving the expression of thousands of genes and many signaling pathways that lead to metabolic changes, such as hydrolysis of macromolecules and a massive remobilization of the hydrolyzed molecules that finally enrich the phloem sap (Buchanan-Wollaston et al. 2003, 2005; Liu et al. 2008). The contention proposed is that the physiological changes in the tissues and particularly in the composition of the phloem sap due to induced senescence have an impact in the aphid’s performance and probing behavior favoring M. persicae, as a higher content of amino acids in the sap could stimulate ingestion.

The induction of senescence by covering the basal part of S. tuberosum plants shortened the prereproductive time of M. persicae nymphs feeding on the apical uncovered leaves (Table 1). On the other hand, induced senescence did not affect the nymph mortality. As such, it can be inferred that the suitability of S. tuberosum (cultivar PO97.11.9) as a host for M. persicae was not affected by dark-induced senescence. Induced senescence also had an impact on M. persicae feeding behavior. This was evident in differences found in EPG phloem phase variables. Aphids spent more time ingesting phloem sap in the apical buds of plants with dark-induced senescence than on control plants, which suggests that induction of senescence promotes aphid ingestion. It has previously been shown that susceptibility or resistance in Solanum genotypes is mostly related to phloem factors (Alvarez 2007; Le Roux et al. 2008, 2010) and that foliar senescence allowed M. persicae to settle on senescent leaves of resistant cultivar Kardal, so it can be inferred that the increased ingestion in senescent-induced plants is related to phloem changes (Alvarez et al. 2014). Aphids performed significantly more test probes after the first sustained E2. The role of these test probes is still unknown, although it has been shown that in their way to the phloem, aphids repeatedly insert their stylets into the mesophyll cells performing brief probes, probably to prepare the tissue for feeding (Tjallingii 1985, 1988, 1995), and it is likely that they do it after sustained feeding. The plant acceptance by aphids was slightly enhanced by the induction of senescence, as the percentage of aphids that reached sustained phloem feeding in plants with dark-induced senescence was higher (82%) than the control plants (60%), although differences did not reach statistical significance. There are reports of aphid—plant interaction showing that modifications of plant physiology benefit aphids. Sandström et al. (2000) found that S. graminum and Diuraphis noxia (Mordvilko) induce chlorotic lesions in their host and thus alter the plant physiology, increasing the concentration of amino acids, especially glutamine. In contrast, Rhopalosiphum padi, which does not induce macroscopic changes in its host plants, seems to have little effect on the amino acid content of host phloem (Sandström et al. 2000). These changes are likely to be nutritionally advantageous for the aphids, but further research of the effect of these changes on aphid fitness is needed. Another example is the black pecan aphid, Melanocallis caryaefoliae (Davis), which feeds on mature and senescent foliage and prefers to settle on leaf discs showing chlorosis from previous feeding by the same aphid than on control discs (Cottrell et al. 2009). On the other hand, it has also been proposed that plants may use senescence as a resistance mechanism. In the Arabidopsis hypersenescent mutant [PR genes5 (cpr 5) hypersenescence1], plant resistance seems to be associated with senescence, as aphids counts were lower and the growth rate was reduced when M. persicae fed on this mutant. However, it is likely that this mutant is not a good host for M. persicae because it expresses senescence constitutively and therefore has a lower chlorophyll content. Furthermore, this mutant spontaneously undergoes cell death (Pegadaraju et al. 2005, 2007). Moreover, it is likely that it does not redistribute and recycle nutrients by manipulating the plant physiology that is necessary for aphid feeding (Sandström et al. 2000; Walling 2000, 2008, 2009; Alvarez 2007; Cottrell et al. 2009).

Table 1.

Prereproductive time of M. persicae (in days) and percent nymphal mortality during the prereproductive period on the apical leaves of senescent and control S. tuberosum plants

t01_01.gif

Table 2.

Mean (±SEM) EPG variables, as means per insect, during 6 h of monitoring of M. persicae probing behavior in the apical leaves of S. tuberosum plants with induced senescence and control plants

t02_01.gif

Covering the leaves with the black cloth proved to be an effective method to induce senescence, as the chlorophyll content was significantly reduced (Fig. 1). There is evidence that shows chlorophyll content can be used to indicate the initiation of senescence and that the regreening ability of etiolated leaves depends on the duration of the dark phase and the plant species (reviewed by van Doom 2005). In Arabidopsis and wheat, etiolation is irreversible after 2 and 4 d of darkness, respectively (Wittenbach 1977, Weaver and Amasino 2001). There have been concerns expressed about the validity of the use of dark-induced senescence as a method to mimic the senescence process because, although many of the events that occur in dark-treated leaves are known to mirror those that occurred in developmental senescence, there also many differences shown as differently expressed genes related to hormone signaling, metabolism and mobilization of nitrogen and lipids, and sugar starvation (Becker and Apel 1993, Weaver et al. 1998, Lin and Wu 2004, Buchanan-Wollaston et al. 2005). Although the limitations of the dark-induction approach should be taken into account, it still seems to be the most appropriate approach for studies on foliar senescence—insect interaction.

In summary, the findings reported here support the hypothesis that plant acceptance by aphids may be improved by foliar senescence and aphids may induce senescence for their own benefit by preparing the tissues for feeding activity, promoting an increase in the nutritional quality of the phloem sap, and coping with phloem resistance factors (Zhu-Salzman et al. 2004; Alvarez 2007; Alvarez et al. 2013). Despite this evidence, it is not clear what mechanism the aphids utilize to induce senescence, although senescence-related genes are upregulated during M. persicae attack on Solanum plants (Alvarez et al. 2013).

Acknowledgments

This research was supported by the Research Council of the National University of Salta, Salta, Argentina. C. Machado-Assefh was founded by a PhD felloship from CONICET. We thank Dr. Freddy Tjallingii for his valuable support of the EPG study. We also thank the anonymous reviewers who helped to improve this article.

References Cited

1.

A. E. Alvarez 2007. Resistance mechanisms of Solanum species to Myzus persicae. Ph.D. dissertation. Wageningen University, The Netherlands, (  http://edepot.wur.nl/25052 ). Google Scholar

2.

A. E. Alvarez , W. F. Tjallingii , E. Garzo , V. Vleeshouwers , M. Dicke , and B. Vosman . 2006. Location of resistance factors in the leaves of potato and wild tuber-bearing Solanum species to the aphid Myzus persicae. Entomol. Exp. Appl. 121: 145–157. Google Scholar

3.

A. E. Alvarez , V. G. Broglia , A. M. Alberti D'Amato , D. Wouters , E. Van der Vossen , E. Garzo , W. Fred Tjallingii , M. Dicke , and B. Vosman . 2013. Comparative analysis of Solanum stoloniferum responses to probing by the green peach aphid, Myzus persicae and the potato aphid, Macrosiphum euphorbiae. Insect Sci. 20: 207–227. Google Scholar

4.

A. E. Alvarez , A. M. Alberti D'Amato , W. F. Tjallingii , M. Dicke , and B. Vosman . 2014. Response of Solanum tuberosum to Myzus persicae infestation at different stages of foliage maturity. (  http://onlinelibrary.wiley.com/journal/10.1111/(ISSN) 1744-7917/earlyview ). Google Scholar

5.

E. A. Backus , A. R. Cline , M. R. Ellerseick , and M. S. Serrano . 2007. Behaviour: Lygus hesperus (Hemiptera: Miridae) feeding on cotton: new methods and parameters for analysis of nonsequential electrical penetration graph data. Ann. Entomol. Soc. Am. 100: 296–310. Google Scholar

6.

W. Becker , and K. Apel . 1993. Differences in gene expression between natural and artificially induced leaf senescence. Planta 189: 74–79. Google Scholar

7.

S. Boquel , P. Giordanengo , and A. Ameline . 2011. Probing behavior of apterous and alate morphs of two potato-colonizing aphids. J. Insect Sci. 11: 164. Google Scholar

8.

E. Breeze , E. Harrison , T. Page , N. Warner , C. Shen , C. Zhang , and V. Buchanan-Wollaston . 2008. Transcriptional regulation of plant senescence: from functional genomics to systems biology. Plant Biol. 10: 99–109. Google Scholar

9.

V. Buchanan-Wollaston 1997. The molecular biology of leaf senescence. J. Exp. Bot. 48: 181–199. Google Scholar

10.

V. Buchanan-Wollaston , S. Earl , E. Harrison , E. Mathas , S. Navabpour , T. Page , and D. Pink . 2003. The molecular analysis of leaf senescence—a genomics approach. Plant Biotechnol. J. 1: 3–22. Google Scholar

11.

V. Buchanan-Wollaston , T. Page , E. Harrison , E. Breeze , P. O. Lim , H. G. Nam , J. F. Lin , S. H. Wu , J. Swidzinski , K. Ishizaki , et al. 2005. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J. 42: 567–585. Google Scholar

12.

A. A. Cherqui , and W.W.F. Tjallingii . 2000. Salivary proteins of aphids, a pilot study on identification, separation and immunolocalization. J. Insect Physiol. 46: 1177–1186. Google Scholar

13.

T. E. Cottrell , B. W. Wood , and X. Ni . 2009. Chlorotic feeding injury by the black pecan aphid (Hemiptera: Aphididae) to pecan foliage promotes aphid settling and nymphal development. Environ. Entomol. 38: 411–416. Google Scholar

14.

M. De Vos , and G. Jander . 2009. Myzus persicae (green peach aphid) salivary components induce defence responses in Arabidopsis thaliana. Plant Cell Environ. 32: 1548–1560. Google Scholar

15.

M. De Vos , V. R. Van Oosten , R.M.P. Van Poecke , J. A. Van Pelt , M. J. Pozo , M. J. Mueller , A. J. Buchala , J. P. Métraux , L. C. Van Loon , M. Dicke , et al. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant Microbe Interact. 18:923–937. Google Scholar

16.

M. De Vos , J. H. Kim , and G. Jander . 2007. Biochemistry and molecular biology of Arabidopsis-aphid interactions. BioEssays 29: 871–883. Google Scholar

17.

J. A. Di-Rienzo , F. Casanoves , M. G. Balzarini , L. Gonzalez , M. Tablada , and C. W. Robledo . 2011. InfoStat versión 2011. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina (  http://www.infostat.com.ar ). Google Scholar

18.

A. E. Douglas 2003. The nutritional physiology of aphids. Adv. Insect Physiol. 31:73–140. Google Scholar

19.

A. Fereres , and A. Moreno . 2009. Behavioural aspects influencing plant virus transmission by homopteran insects. Virus Res. 141: 158–168. Google Scholar

20.

S. S. Gepstein , G. G. Sabehi , M. M. CarpJ , T. T. Hajouj , M.M.F.O. Nesher , I. Yariv , C. Dor , and M. Bassani . 2003. Large-scale identification of leaf senescence-associated genes. Plant J. 36: 629–642. Google Scholar

21.

Y. He , H. Fukushige , D. F. Hildebrand , and S. Gan . 2002. Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol. 128:876–884. Google Scholar

22.

K. Kamachi , T. Yamaya , T. Hayakawa , T. Mae , and K. Ojima . 1992. Changes in cytosolic glutamine synthetase polypeptide and its mRNA in a leaf blade of rice plants during natural senescence. Plant Physiol. 98: 1323–1329. Google Scholar

23.

G. Kuroli , and Z. S. Lantos . 2006. Long-term study of alata aphid flight activity and abundance of potato colonizing aphid species. Acta Phytopathol. Entomol. Hung. 41: 261–273. Google Scholar

24.

V. Le Roux , S. Dugravot , E. Campan , F. Dubois , C. Vincent , and P. Giordanengo . 2008. Wild Solanum resistance to aphids: antixenosis or antibiosis? J. Econ. Entomol. 101: 584–591. Google Scholar

25.

V. Le Roux , S. Dugravot , L. Brunissen , C. Vincent , Y. Pelletier , and P. Giordanengo . 2010. Antixenosis phloem-based resistance to aphids: is it the rule? Ecol. Entomol. 35: 407–416. Google Scholar

26.

H. K. Lichtenthaler 1987. Chlorophyll and carotenoids: pigments of photosynthetic biomembranes. In R. D. Lester Packer (ed.), Methods in Enzymology. Academic Press. Google Scholar

27.

P. O. Lim , H. J. Kim , and H. G. Nam . 2007. Leaf senescence. Annu. Rev. Plant Biol. 58: 115–136. Google Scholar

28.

J. F. Lin , and S. H. Wu . 2004. Molecular events in senescing Arabidopsis leaves. Plant J. 39: 612–628. Google Scholar

29.

J. Liu , H. W. Yun , J. Y. Jun , D. L. Yu , and F. S. Fa . 2008. Protein degradation and nitrogen remobilization during leaf senescence. J. Plant Biol. 51: 11–19. Google Scholar

30.

B. Martin , J. L. Collar , W. F. Tjallingii , and A. Fereres . 1997. Intracellular ingestion and salivation by aphids may cause the acquisition and inoculation of non-persistently transmitted plant viruses. J. Gen. Virol. 78: 2701–2705. Google Scholar

31.

D. L. McLean , and M. G. Kinsey 1964. A technique for electronically recording aphid feeding and salivation. Nature 202: 1358–1359. Google Scholar

32.

P. W. Miles 1999. Aphid saliva. Biol. Rev. Camb. Philos. Soc. 74: 41–85. Google Scholar

33.

P. J. Moran , and G. A. Thompson . 2001. Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. Plant Physiol. 125: 1074–1085. Google Scholar

34.

P. J. Moran , Y. Cheng , J. Cassell , and G. A. Thompson . 2002. Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. Arch. Insect Biochem. Physiol. 51: 182–203. Google Scholar

35.

T. Page , G. Griffiths , and V. Buchanan-Wollaston . 2001. Molecular and biochemical characterization of postharvest senescence in broccoli. Plant Physiol. 125: 718–727. Google Scholar

36.

V. Pegadaraju , C. Knepper , J. Reese , and J. Shah . 2005. Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid. Plant Physiol. 139: 1927–1934. Google Scholar

37.

V. Pegadaraju , J. Louis , V. Singh , J. C. Reese , J. Bautor , B. J. Feys , G. Cook , J. E. Parker , and J. Shah . 2007. Phloem-based resistance to green peach aphid is controlled by Arabidopsis PHYTOALEXIN DEFICIENT4 without its signaling partner ENHANCED DISEASE SUSCEPTIBILITY 1. Plant J. 52:332–341. Google Scholar

38.

D. G. Pollard 1973. Plant penetration by feeding aphids (Hemiptera, Aphidoidea): a review. Bull. Entomol. Res. 62: 631–714. Google Scholar

39.

R. J. Porra , W. A. Thompson , and P. E. Kriedemann . 1989. Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim. Biophy. Acta 975: 384–394. Google Scholar

40.

E. Prado , and W. F. Tjallingii . 2007. Behavioral evidence for local reduction of aphid-induced resistance. J. Insect Sci. 7: 48. Google Scholar

41.

J. Sandström , A. Telang , and N. A. Moran . 2000. Nutritional enhancement of host plants by aphids—a comparison of three aphid species on grasses. J. Insect Physiol. 46: 33–10. Google Scholar

42.

E. Sarria , M. Cid , E. Garzo , and A. Fereres . 2009. Excel Workbook for automatic parameter calculation of EPG data. Comput. Electron. Agric. 67: 35–42. Google Scholar

43.

W. F. Tjallingii 1978. Electronic recording of penetration behaviour by aphids. Entomol. Exp. Appl. 24: 721–730. Google Scholar

44.

W. F. Tjallingii 1985. Electrical nature of recorded signals during stylet penetration by aphids. Entomol. Exp. Appl. 38: 177–186. Google Scholar

45.

W. F. Tjallingii 1988. Electrical recording of stylet penetration activities, pp. 95–108. In A. K. Minks and P. Harrewijn (eds.), Aphids, their biology, natural enemies and control. Elsevier, Amsterdam. Google Scholar

46.

W. F. Tjallingii 1990a. Continuous recording of stylet penetration activities by aphids, pp. 89–99. In R. K. Campbell and R. D. Eikenbary (eds.), Aphidplant genotype interactions. Elsevier, Amsterdam. Google Scholar

47.

W. F. Tjallingii 1990b. Stylet penetration parameters from aphids in relation to host-plant resistance. Symp. Biol. Hung. 39: 411–419. Google Scholar

48.

W. F. Tjallingii 1995. Aphid-plant interactions: what goes on in the depth of the tissues? Proc. Exp. Appl. Entomol. 6: 163–169. Google Scholar

49.

W. F. Tjallingii 2006. Salivary secretions by aphids interacting with proteins of phloem wound responses. J. Exp. Bot. 57: 739–745. Google Scholar

50.

W. F. Tjallingii , and T. Hogen Esch . 1993. Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol. Entomol. 18: 189–200. Google Scholar

51.

W. F. Tjallingii , E. Garzo , and A. Fereres . 2010. New structure in cell puncture activities by aphid stylets: a dual-mode EPG study. Entomol. Exp. Appl. 135: 193–207. Google Scholar

52.

W. G. van Doorn 2005. Plant programmed cell death and the point of no return. Trends Plant Sci. 10: 478–483. Google Scholar

53.

L. L. Walling 2000. The myriad plant responses to herbivores. J. Plant Growth Regul. 19: 195–216. Google Scholar

54.

L. L. Walling 2008. Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol. 146: 859–866. Google Scholar

55.

L. L. Walling 2009. Adaptive defense responses to pathogens and insects. Plant Innate Immun. 51:551–612. Google Scholar

56.

A. Watanabe , N. Takagi , H. Hayashi , M. Chino , and A. Watanabe . 1997. Internal Gln/Glu ratio as a potential regulatory parameter for the expression of a cytosolic glutamine synthetase gene of radish in cultured cells. Plant Cell Physiol. 38: 1000–1026. Google Scholar

57.

L. Weaver , S. Gan , B. Quirino , and R. Amasino . 1998. A comparison of the expression patterns of several senescence-associated genes in response to stress and hormone treatment. Plant Mol. Biol. 37: 455–469. Google Scholar

58.

L. M. Weaver , and R. M. Amasino . 2001. Senescence is induced in individually darkened Arabidopsis leaves, but inhibited in whole darkened plants. Plant Physiol. 127: 876–886. Google Scholar

59.

T. Will , and A.J.E. van Bel . 2006. Physical and chemical interactions between aphids and plants. J. Exp. Bot. 57: 729–737. Google Scholar

60.

V. A. Wittenbach 1977. Induced senescence of intact wheat seedlings and its reversibility. Plant Physiol. 59: 1039–1042. Google Scholar

61.

K. Zhu-Salzman , R. A. Salzman , J. E. Ahn , and H. Koiwa . 2004. Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiol. 134: 420–431. Google Scholar

Notes

[1] This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

© The Author 2014. Published by Oxford University Press on behalf of the Entomological Society of America.
Cristina R. Machado-Assefh, Alejandro F. Lucatti, and Adriana E. Alvarez "Induced Senescence Promotes the Feeding Activities and Nymph Development of Myzus persicae (Hemiptera: Aphididae) on Potato Plants," Journal of Insect Science 14(155), 1-6, (1 January 2014). https://doi.org/10.1093/jisesa/ieu017
Received: 30 November 2012; Accepted: 26 April 2013; Published: 1 January 2014
JOURNAL ARTICLE
6 PAGES


Share
SHARE
KEYWORDS
electrical penetration graph
green peach aphid
Solanum tuberosum
RIGHTS & PERMISSIONS
Get copyright permission
Back to Top